Effects of restraint stress on NALT structure and nasal IgA levels

Immunology Letters

Volumn 135, Issue 1-2, 2011, Pages 78-87

  Oros Pantoja, Rigoberto ^a   Jarillo Luna, Adriana ^a   Rivera Aguilar, Víctor ^b   Sánchez Torres, Luvia Enid ^a   Godinez Victoria, Marycarmen ^a   Campos Rodríguez, Rafael ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Catecholamines; Glucocorticoids; IgA; Lymphocytes; NALT; Restraint stress

Indexed keywords

CORTICOSTERONE; IMMUNOGLOBULIN A; NORADRENALIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BAGG ALBINO MOUSE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORTICOSTEROID BLOOD LEVEL; FLOW CYTOMETRY; IMMOBILIZATION STRESS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; LYMPHOID TISSUE; MALE; MOUSE; MUCOSAL IMMUNITY; NASAL ASSOCIATED LYMPHOID TISSUE; NONHUMAN; NORADRENALIN BLOOD LEVEL; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ANIMALS; ANTIGENS, CD; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CORTICOSTERONE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; MALE; MICE; MICE, INBRED BALB C; NASAL MUCOSA; NOREPINEPHRINE; RESTRAINT, PHYSICAL; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 78751701914     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2010.10.001     Document Type: Article

References (77)

1. Mayer E.A. Psychological stress and colitis. Gut 2000, 46:595-596.
2. Mayer E.A. The neurobiology of stress and gastrointestinal disease. Gut 2000, 47:861-869.
3. Mayer E.A., Naliboff B.D., Chang L., Coutinho S.V.V. Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2001, 280:G519-524.
4. Collins S.M. Stress and the gastrointestinal tract IV. Modulation of intestinal inflammation by stress: basic mechanisms and clinical relevance. Am J Physiol Gastrointest Liver Physiol 2001, 280:G315-G318.
5. Mawdsley J.E., Rampton D.S. Psychological stress in IBD: new insights into pathogenic and therapeutic implications. Gut 2005, 54:1481-1491.
6. Pedersen B.K., Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000, 80:1055-1081.
7. Gleeson M., Bishop N.C. Special feature for the Olympics: effects of exercise on the immune system: modification of immune responses to exercise by carbohydrate, glutamine and anti-oxidant supplements. Immunol Cell Biol 2000, 78:554-561.
8. Gleeson M., Pyne D.B. Special feature for the Olympics: effects of exercise on the immune system: exercise effects on mucosal immunity. Immunol Cell Biol 2000, 78:536-544.
9. Pyne D.B., McDonald W.A., Gleeson M., Flanagan A., Clancy R.L., Fricker P.A. Mucosal immunity, respiratory illness, and competitive performance in elite swimmers. Med Sci Sports Exerc 2001, 33:348-353.
10. Bosch J.A., Ring C., de Geus E.J., Veerman E.C., Amerongen A.V. Stress and secretory immunity. Int Rev Neurobiol 2002, 52:213-253.
11. Teeuw W., Bosch J.A., Veerman E.C., Amerongen A.V. Neuroendocrine regulation of salivary IgA synthesis and secretion: implications for oral health. Biol Chem 2004, 385:1137-1146.
12. Jarillo-Luna A., Rivera-Aguilar V., Garfias H.R., Lara-Padilla E., Kormanovsky A., Campos-Rodriguez R. Effect of repeated restraint stress on the levels of intestinal IgA in mice. Psychoneuroendocrinology 2007, 32:681-692.
13. Jarillo-Luna A., Rivera-Aguilar V., Martinez-Carrillo B.E., Barbosa-Cabrera E., Garfias H.R., Campos-Rodriguez R. Effect of restraint stress on the population of intestinal intraepithelial lymphocytes in mice. Brain Behav Immun 2007.
14. Cohen S., Tyrrell D.A., Smith A.P. Psychological stress and susceptibility to the common cold. N Engl J Med 1991, 325:606-612.
15. Bermon S. Airway inflammation and upper respiratory tract infection in athletes: is there a link?. Exerc Immunol Rev 2007, 13:6-14.
16. Gleeson M. Mucosal immunity and respiratory illness in elite athletes. Int J Sports Med 2000, 21(Suppl. 1):S33-S43.
17. Gleeson M. Mucosal immune responses and risk of respiratory illness in elite athletes. Exerc Immunol Rev 2000, 6:5-42.
18. Nieman D.C. Exercise, infection, and immunity. Int J Sports Med 1994, 15(Suppl. 3):S131-S141.
19. Gleeson M., McDonald W.A., Pyne D.B., Cripps A.W., Francis J.L., Fricker P.A., et al. Salivary IgA levels and infection risk in elite swimmers. Med Sci Sports Exerc 1999, 31:67-73.
20. Gleeson M., McDonald W.A., Pyne D.B., Clancy R.L., Cripps A.W., Francis J.L., et al. Immune status and respiratory illness for elite swimmers during a 12-week training cycle. Int J Sports Med 2000, 21:302-307.
21. Mackinnon L. Advances in Exercise Immunology. Human Kinetics 1999.
22. Sheridan J.F., Dobbs C., Jung J., Chu X., Konstantinos A., Padgett D., et al. Stress-induced neuroendocrine modulation of viral pathogenesis and immunity. Ann N Y Acad Sci 1998, 840:803-808.
23. Nishioka K., Okano M., Ichihara Y., Ichihara N., Nishizaki K. Immunosuppressive effect of restraint stress on the initiation of allergic rhinitis in mice. Int Arch Allergy Immunol 2005, 136:142-147.
24. Boudreau J., Quadrilatero J., Hoffman-Goetz L. Voluntary training in mice and submandibular lymphocyte response to acute exercise. Med Sci Sports Exerc 2005, 37:2038-2045.
25. Quadrilatero J., Boudreau J., Hoffman-Goetz L. Lymphocyte distribution in mouse submandibular lymph nodes in response to acute treadmill exercise. Can J Physiol Pharmacol 2003, 81:972-978.
26. Csencsits K.L., Jutila M.A., Pascual D.W. Nasal-associated lymphoid tissue: phenotypic and functional evidence for the primary role of peripheral node addressing in naive lymphocyte adhesion to high endothelial venules in a mucosal site. J Immunol 1999, 163:1382-1389.
27. Bienenstock J., McDermott M.R. Bronchus- and nasal-associated lymphoid tissues. Immunol Rev 2005, 206:22-31.
28. Kraal G. Nasal-associated lymphoid tissue. Mucosal immunology 2005, 415-422. Elsevier, Amsterdam. J. Mestecky, M.E. Lamm, W. Strober, J. Bienenstock, J.R. McGhee, L. Mayer (Eds.).
29. Kiyono H., Fukuyama S. NALT- versus Peyer's-patch-mediated mucosal immunity. Nat Rev Immunol 2004, 4:699-710.
30. Asanuma H., Thompson A.H., Iwasaki T., Sato Y., Inaba Y., Aizawa C., et al. Isolation and characterization of mouse nasal-associated lymphoid tissue. J Immunol Methods 1997, 202:123-131.
31. Heritage P.L., Underdown B.J., Arsenault A.L., Snider D.P., McDermott M.R. Comparison of murine nasal-associated lymphoid tissue and Peyer's patches. Am J Respir Crit Care Med 1997, 156:1256-1262.
32. Rodriguez-Monroy M.A., Rojas-Hernandez S., Moreno-Fierros L. Phenotypic and functional differences between lymphocytes from NALT and nasal passages of mice. Scand J Immunol 2007, 65:276-288.
33. Dhabhar F.S., McEwen B.S., Spencer R.L. Adaptation to prolonged or repeated stress-comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology 1997, 65:360-368.
34. Strausbaugh H.J., Dallman M.F., Levine J.D. Repeated, but not acute, stress suppresses inflammatory plasma extravasation. Proc Natl Acad Sci U S A 1999, 96:14629-14634.
35. Melia K.R., Ryabinin A.E., Schroeder R., Bloom F.E., Wilson M.C. Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J Neurosci 1994, 14:5929-5938.
36. Armario A., Hidalgo J., Giralt M. Evidence that the pituitary-adrenal axis does not cross-adapt to stressors: comparison to other physiological variables. Neuroendocrinology 1988, 47:263-267.
37. Hashimoto K., Suemaru S., Takao T., Sugawara M., Makino S., Ota Z. Corticotropin-releasing hormone and pituitary-adrenocortical responses in chronically stressed rats. Regul Pept 1988, 23:117-126.
38. Hauger R.L., Lorang M., Irwin M., Aguilera G. CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Res 1990, 532:34-40.
39. Ma X.M., Lightman S.L. The arginine vasopressin and corticotrophin-releasing hormone gene transcription responses to varied frequencies of repeated stress in rats. J Physiol 1998, 510(Pt 2):605-614.
40. Ma X.M., Lightman S.L., Aguilera G. Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint. Endocrinology 1999, 140:3623-3632.
41. Andres R., Marti O., Armario A. Direct evidence of acute stress-induced facilitation of ACTH response to subsequent stress in rats. Am J Physiol 1999, 277:R863-R868.
42. Gadek-Michalska A., Bugajski J. Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J Physiol Pharmacol 2003, 54:449-459.
43. Dallman M.F., Akana S.F., Strack A.M., Scribner K.S., Pecoraro N., La Fleur S.E., et al. Chronic stress-induced effects of corticosterone on brain: direct and indirect. Ann N Y Acad Sci 2004, 1018:141-150.
44. Rich E.L., Romero L.M. Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Physiol Regul Integr Comp Physiol 2005, 288:R1628-R1636.
45. Uresin Y., Erbas B., Ozek M., Ozkok E., Gurol A.O. Losartan may prevent the elevation of plasma glucose, corticosterone and catecholamine levels induced by chronic stress. J Renin Angiotensin Aldosterone Syst 2004, 5:93-96.
46. Durnova G.N., Kaplanskii A.S., Glagoleva E.V. Dynamics of morphological changes in the adrenal glands and lymphoid organs during immobilization stress in rats. Arkh Anat Gistol Embriol 1983, 85:67-72.
47. Grigorenko D.E., Budushkina E.E. Mesenteric lymph nodes in the rat after exposure to hydrocortisone. Arkh Anat Gistol Embriol 1985, 89:58-62.
48. Dominguez-Gerpe L., Rey-Mendez M. Time-course of the murine lymphoid tissue involution during and following stressor exposure. Life Sci 1997, 61:1019-1027.
49. Sudo N., Oyama N., Yu X.N., Kubo C. Restraint stress-induced elevation of endogenous glucocorticoids decreases Peyer's patch cell numbers via mechanisms that are either dependent or independent on apoptotic cell death. Neuroimmunomodulation 2001, 9:333-339.
50. Roy M.J., Walsh T.J. Histopathologic and immunohistochemical changes in gut-associated lymphoid tissues after treatment of rabbits with dexamethasone. Lab Invest 1992, 66:437-443.
51. Kiank C., Holtfreter B., Starke A., Mundt A., Wilke C., Schutt C. Stress susceptibility predicts the severity of immune depression and the failure to combat bacterial infections in chronically stressed mice. Brain Behav Immun 2006, 20:359-368.
52. Gonzales X.F., Deshmukh A., Pulse M., Johnson K., Jones H.P. Stress-induced differences in primary and secondary resistance against bacterial sepsis corresponds with diverse corticotropin releasing hormone receptor expression by pulmonary CD11c+ MHC II+ and CD11c- MHC II+ APCs. Brain Behav Immun 2008, 22:552-564.
53. Bauer M.E., Perks P., Lightman S.L., Shanks N. Are adhesion molecules involved in stress-induced changes in lymphocyte distribution?. Life Sci 2001, 69:1167-1179.
54. Sudo N., Yu X.N., Sogawa H., Kubo C. Restraint stress causes tissue-specific changes in the immune cell distribution. Neuroimmunomodulation 1997, 4:113-119.
55. Yin D., Tuthill D., Mufson R.A., Shi Y. Chronic restraint stress promotes lymphocyte apoptosis by modulating CD95 expression. J Exp Med 2000, 191:1423-1428.
56. Teshima H., Sogawa H., Kihara H., Nakagawa T. Influence of stress on the maturity of T-cells. Life Sci 1991, 49:1571-1581.
57. Sminia T.K.G. Nasal-associated lymphoid tissue. Mucosal Immunol 1999, 357-364.
58. Cesta M.F. Normal structure, function, and histology of mucosa-associated lymphoid tissue. Toxicol Pathol 2006, 34:599-608.
59. Winther B., Innes D.J., Mills S.E., Mygind N., Zito D., Hayden F.G. Lymphocyte subsets in normal airway mucosa of the human nose. Arch Otolaryngol Head Neck Surg 1987, 113:59-62.
60. Graeme-Cook F., Bhan A.K., Harris N.L. Immunohistochemical characterization of intraepithelial and subepithelial mononuclear cells of the upper airways. Am J Pathol 1993, 143:1416-1422.
61. Hameleers D.M., Stoop A.E., van der Ven I., Biewenga J., van der Baan S., Sminia T. Intra-epithelial lymphocytes and non-lymphoid cells in the human nasal mucosa. Int Arch Allergy Appl Immunol 1989, 88:317-322.
62. Pawankar R., Okuda M. A comparative study of the characteristics of intraepithelial and lamina propria lymphocytes of the human nasal mucosa. Allergy 1993, 48:99-105.
63. Okuda M., Pawankar R. Flow cytometric analysis of intraepithelial lymphocytes in the human nasal mucosa. Allergy 1992, 47:255-259.
64. Coutinho H.B., Robalinho T.I., Coutinho V.B., Amorim A.M., Furtado A.F., Ferraz A., et al. Intra-abdominal sepsis: an immunocytochemical study of the small intestine mucosa. J Clin Pathol 1997, 50:294-298.
65. Nilssen D.E., Oktedalen O., Lygren I., Opstad P.K., Brandtzaeg P. Intestinal IgA- and IgM-producing cells are not decreased in marathon runners. Int J Sports Med 1998, 19:425-431.
66. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000, 52:595-638.
67. + T and B lymphocyte function in vitro and in vivo. Pharmacol Rev 2001, 53:487-525.
68. Sanders V.M., Kohm A.P. Sympathetic nervous system interaction with the immune system. Int Rev Neurobiol 2002, 52:17-41.
69. Li Y.S., Kouassi E., Revillard J.P. Differential regulation of mouse B-cell activation by beta-adrenoceptor stimulation depending on type of mitogens. Immunology 1990, 69:367-372.
70. Winzer A., Ring C., Carroll D., Willemsen G., Drayson M., Kendall M. Secretory immunoglobulin A and cardiovascular reactions to mental arithmetic, cold pressor, and exercise: effects of beta-adrenergic blockade. Psychophysiology 1999, 36:591-601.
71. Bergquist J., Tarkowski A., Ewing A., Ekman R. Catecholaminergic suppression of immunocompetent cells. Immunol Today 1998, 19:562-567.
72. Stevenson J.R., Westermann J., Liebmann P.M., Hortner M., Rinner I., Felsner P., et al. Prolonged alpha-adrenergic stimulation causes changes in leukocyte distribution and lymphocyte apoptosis in the rat. J Neuroimmunol 2001, 120:50-57.
73. Benschop R.J., Rodriguez-Feuerhahn M., Schedlowski M. Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav Immun 1996, 10:77-91.
74. Gader A.M., Cash J.D. The effect of adrenaline, noradrenaline, isoprenaline and salbutamol on the resting levels of white blood cells in man. Scand J Haematol 1975, 14:5-10.
75. Gonzalez-Ariki S., Husband A.J. The role of sympathetic innervation of the gut in regulating mucosal immune responses. Brain Behav Immun 1998, 12:53-63.
76. Schmidt P.T., Eriksen L., Loftager M., Rasmussen T.N., Holst J.J. Fast acting nervous regulation of immunoglobulin A secretion from isolated perfused porcine ileum. Gut 1999, 45:679-685.
77. Lundgren O. Sympathetic input into the enteric nervous system. Gut 2000, 47(Suppl. 4):iv33-35. [discussion iv36].